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Extremely acidic proteomes and metabolic flexibility in bacteria and highly diversified archaea thriving in geothermal chaotropic brines

Nature Ecology & Evolution (2024)Cite this article

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Abstract

Few described archaeal, and fewer bacterial, lineages thrive under salt-saturating conditions, such as solar saltern crystallizers (salinity above 30% w/v). They accumulate molar K+ cytoplasmic concentrations to maintain osmotic balance (‘salt-in’ strategy) and have proteins adaptively enriched in negatively charged acidic amino acids. Here we analysed metagenomes and metagenome-assembled genomes from geothermally influenced hypersaline ecosystems with increasing chaotropicity in the Danakil Depression. Normalized abundances of universal single-copy genes confirmed that haloarchaea and Nanohaloarchaeota encompass 99% of microbial communities in the near-life-limiting conditions of the Western-Canyon Lakes. Danakil metagenome- and metagenome-assembled-genome-inferred proteomes, compared with those of freshwater, seawater and solar saltern ponds up to saturation (6–14–32% salinity), showed that Western-Canyon Lake archaea encode the most acidic proteomes ever observed (median protein isoelectric points ≤4.4). We identified previously undescribed haloarchaeal families as well as an Aenigmatarchaeota family and a bacterial phylum independently adapted to extreme halophily. Despite phylum-level diversity decreasing with increasing salinity–chaotropicity, and unlike in solar salterns, adapted archaea exceedingly diversified in Danakil ecosystems, challenging the notion of decreasing diversity under extreme conditions. Metabolic flexibility to utilize multiple energy and carbon resources generated by local hydrothermalism along feast-and-famine strategies seemingly shapes microbial diversity in these ecosystems near life limits.

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Fig. 1: Microbial community composition inferred from metagenomes of polyextreme chaotropic ecosystems in the north Danakil Depression.
Fig. 2: pI and amino acid compositional biases of inferred proteomes for microorganisms thriving in increasingly chaotropic ecosystems from the north Danakil Depression.
Fig. 3: Diversity indexes for all species and dominant archaeal taxa in Danakil geothermally influenced chaotropic brines compared with other ecosystems of increasing salinity.
Fig. 4: Phylogenomic trees of newly identified archaeal and bacterial MAGs in hypersaline chaotropic north Danakil ecosystems.
Fig. 5: Major processes involved in energy metabolism in microbial communities from Danakil polyextreme brine ecosystems.

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Data availability

Metagenomes and MAGs are available in GenBank under Bioproject PRJNA541281. The accession numbers for individual metagenomes are SAMN37693137 (DAL-Ass), SAMN37693138 (DAL-9Ass), SAMN37693139 (DAL-9Gt), SAMN37693140 (DAL-WCL2) and SAMN37693141 (DAL-WCL3). Accession numbers for MAGs are provided in Supplementary Table 5. Reference databases used include Pfam-A database v.3.1b2 (http://pfam.xfam.org/), UniProtKB-SwissProt (05.2022); https://www.expasy.org/resources/uniprotkb-swiss-prot), KOfams developed by KEGG (https://www.genome.jp/tools/kofamkoala/), GTDB r214 (https://gtdb.ecogenomic.org/) and CAZyDB (release 09242021; http://www.cazy.org/).

Code availability

Custom code for these analyses (perl and R scripts) is available via GitLab at https://gitlab.com/DeemTeam/dal-metagenomes.

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Acknowledgements

We thank F. Brenckman and the Iris Foundation for supporting our initial field trip in 2016 and the Mamont Foundation, for field trip support in 2019. We thank J. Belilla, J. M. López-García, A. I. López-Archilla, K. Benzerara, L. Jardillier, O. Grunewald, L. Cantamessa and the Afar authorities for their assistance during field trips and P. Deschamps for help with software installation. This work was supported by the Moore-Simons Project on the Origin of the Eukaryotic Cell (P.L.-G., https://doi.org/10.37807/GBMF9739), the Iris Foundation (P.L.-G., https://en.fondationiris.org/) and the European Research Council Starting Grant Macro-Epik (L.E., no. 803151) and Advanced Grant Plast-Evol (D.M., no. 787904).

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Authors and Affiliations

  1. Ecologie Systématique Evolution, CNRS, Université Paris-Saclay, AgroParisTech, Gif-sur-Yvette, France

    Ana Gutiérrez-Preciado, Bledina Dede, Brittany A. Baker, Laura Eme, David Moreira & Purificación López-García

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Contributions

P.L.-G. and D.M. organized the field trips, collected and conditioned samples, designed the research and obtained funding to conduct it. A.G.-P. carried out the bioinformatic, phylogenetic and statistical analyses from raw metagenome data. B.D. and A.G.-P. investigated genes involved in metabolism. B.B. and L.E. carried out the final phylogenomic analysis for Halobacteria and Nanohaloarchaeota. P.L.-G. conceptualized and supervised the research, and wrote the manuscript. All authors read and commented on the manuscript.

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Correspondence to Purificación López-García.

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Nature Ecology & Evolution thanks Ibrahim Farag, Eric Weingarten and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 Genus-level composition of dominant archaeal phyla in polyextreme ecosystems in the north Danakil Depression.

a, Composition of members ascribing to the Halobacteriota. b, Composition of members ascribing to the Nanohaloarchaeota. Classification according to GTDB r214.

Extended Data Fig. 2 Arginine preference over lysine in north Danakil extreme halophilic communities.

a, Percentage of arginine and lysine in proteomes inferred from Danakil polyextreme ecosystems in comparison with representative ecosystems along a salinity gradient. b, Jitter plot showing Arg/Lys (R/K) ratio inferred from MAGs of Danakil chaotropic brines classified by major taxa. Tukey HSD one-sided test performed to compare those values for the indicated pairs of taxa. ***p-value < 0.001, ****p-value < 0.0001. Statistical details are shown in Supplementary Table 4.

Extended Data Fig. 3 Isoelectric point (pI) and amino acid biases in MAGs assembled from polyextreme brines in the north Danakil Depression.

a, Distribution of pI values in individual MAGs assembled from Lake Assale (Ass, 9Ass), cave reservoir La Grotte (9Gt) and Western Canyon Lakes (WCLs) metagenomes. b, PCA of amino acid composition and individual MAGs retrieved from polyextreme north Danakil ecosystems. c, Asp-Glu/Ile-Lys (DE/IK) ratio in the assembled MAGs. MAGs are colored according to their taxonomic affiliation. Symbol shapes denote the type of hypersaline ecosystem the MAGs were assembled from.

Extended Data Fig. 4 Isoelectric point of proteomes inferred for archaeal and bacterial lineages present in north Danakil hypersaline systems independently adapted to hypersaline conditions.

a, Distribution of pI values in individual MAGs belonging to the Aenigmarchaeota order PWEA01, including the Dallol area MAGs (reddish color), and its phylogenetic relatives (blue colors) as reference. b, Violin plots showing pI values for Danakil MAGs belonging to the Bacteroidota, including references for comparison. Note the low pI values characteristic of the extremely halophilic Salinibacteraceae. c, Distribution of pI values shown by curves (left) and violin plot (right) of MAGs ascribing to the phylum T1Sed10-126 (Candidatus Salsurabacteriota), including the three genomes assembled from the Dallol area ecosystems and the two existing reference genomes from GTDB. The black dot in the violin plots shown in b-c depicts the median.

Extended Data Fig. 5 Heat maps showing major metabolic potential functions and KEGG pathways for individual Halobacteria MAGs assembled from north Danakil hypersaline ecosystems.

a, Presence (blue)-absence (white) of metabolic functions as inferred by Metabolic G in Danakil MAGs and representative GTDB genomes of Halobacteria. b, Modules of KEGG pathways identified in Halobacteria MAGs and GTDB reference genomes (outgroup). The blue color intensity indicates the completeness of the respective pathway (intense, complete). The names of our MAGs are highlighted in red. Aa, amino acid.

Extended Data Fig. 6 Relative abundance and phylogenetic classification of key genes of the reverse tricarboxylic acid (rTCA) and Wood-Ljungdahl C fixation pathways in Danakil metagenomes.

2-oxoglutarate synthase, pyruvate synthase and citrate lyase are characteristic rTCA enzymes; the CO dehydrogenase/acetyl-CoA synthase is considered diagnostic for the Wood-Ljungdahl pathway.

Extended Data Fig. 7 Heat maps showing major metabolic potential functions and KEGG pathways for individual Nanohaloarchaeota MAGs assembled from north Danakil hypersaline ecosystems.

a, Presence (blue)-absence (white) of metabolic functions as inferred by Metabolic G in Danakil MAGs and representative GTDB genomes of Nanohaloarchaeota. b, Modules of KEGG pathways identified in Nanohaloarchaeota MAGs and GTDB reference genomes (outgroup). The blue color intensity indicates the completeness of the pathway. The names of our MAGs are highlighted in orange. Aa, amino acid; ox. phosphor., oxidative phosphorylation.

Extended Data Fig. 8 Heat maps showing major metabolic potential functions and KEGG pathways for MAGs of the halophilic candidate bacterial phylum Salsurabacteriota (T1Sed10-126).

a, Presence-absence of metabolic functions as inferred by Metabolic G in the two most complete Danakil MAGs and known GTDB genomes. b, Modules of KEGG pathways identified in Salsurabacteriota. The names of our MAGs are highlighted in green.

Extended Data Fig. 9 Heat map showing the relative abundance of genes encoding enzymes involved in the degradation of hydrocarbons (alkanes and haloalkanes) and carbohydrates in metagenomes from north Danakil hypersaline ecosystems.

GH, glycoside hydrogenases (involved in carbohydrate degradation).

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This file contains Supplementary Figs. 1–13 and Tables 1–7 in pdf format. Additional Supplementary Tables 8–13 are too large and are provided in a combined Excel file with all tables.

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Gutiérrez-Preciado, A., Dede, B., Baker, B.A. et al. Extremely acidic proteomes and metabolic flexibility in bacteria and highly diversified archaea thriving in geothermal chaotropic brines. Nat Ecol Evol (2024). https://doi.org/10.1038/s41559-024-02505-6

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